VEGF-dependent plasticity of fenestrated capillaries in the normal adult microvasculature

American Journal of Physiology - Heart and Circulatory Physiology - Tập 290 Số 2 - Trang H560-H576 - 2006
Tomomi Kamba1, Betty Y. Tam, Hiroya Hashizume, Amy Haskell, Barbara Sennino, Michael R. Mancuso, Scott M. Norberg, Shaun O’Brien, Rebecca Davis, Lori Morton, Keith D. Anderson, Gavin Thurston, Shuji Joho, Matthew L. Springer, Calvin J. Kuo, Donald M. McDonald
1Cardiovascular Research Institute, and Dept. of Anatomy, Univ. of California, 513 Parnassus Ave., San Francisco, CA 94143-0452, USA.

Tóm tắt

Unlike during development, blood vessels in the adult are generally thought not to require VEGF for normal function. However, VEGF is a survival factor for many tumor vessels, and there are clues that some normal blood vessels may also depend on VEGF. In this study, we sought to identify which, if any, vascular beds in adult mice depend on VEGF for survival. Mice were treated with a small-molecule VEGF receptor (VEGFR) tyrosine kinase inhibitor or soluble VEGFRs for 1–3 wk. Blood vessels were assessed using immunohistochemistry or scanning or transmission electron microscopy. In a study of 17 normal organs after VEGF inhibition, we found significant capillary regression in pancreatic islets, thyroid, adrenal cortex, pituitary, choroid plexus, small-intestinal villi, and epididymal adipose tissue. The amount of regression was dose dependent and varied from organ to organ, with a maximum of 68% in thyroid, but was less in normal organs than in tumors in RIP-Tag2-transgenic mice or in Lewis lung carcinoma. VEGF-dependent capillaries were fenestrated, expressed high levels of both VEGFR-2 and VEGFR-3, and had normal pericyte coverage. Surviving capillaries in affected organs had fewer fenestrations and less VEGFR expression. All mice appeared healthy, but distinct physiological changes, including more efficient blood glucose handling, accompanied some regimens of VEGF inhibition. Strikingly, most capillaries in the thyroid grew back within 2 wk after cessation of treatment for 1 wk. Our findings of VEGF dependency of normal fenestrated capillaries and rapid regrowth after regression demonstrate the plasticity of the adult microvasculature.

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Tài liệu tham khảo

10.1152/ajpendo.00199.2002

10.1016/j.bbrc.2004.08.237

10.1038/nm1095-1024

10.1016/S0165-6147(98)01211-5

10.1161/01.RES.0000125295.43813.1F

10.1016/S0002-9440(10)63540-7

Benjamin LE, Hemo I, and Keshet E.A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF.Development125: 1591–1598, 1998.

Bicknell Rand Harris AL.Anticancer strategies involving the vasculature: vascular targeting and the inhibition of angiogenesis.Semin Cancer Biol3: 399–407, 1992.

10.1096/fj.02-0557fje

10.1073/pnas.101564798

10.1038/380435a0

10.1055/s-2000-13213

10.1093/emboj/21.8.1939

Drevs J, Muller-Driver R, Wittig C, Fuxius S, Esser N, Hugenschmidt H, Konerding MA, Allegrini PR, Wood J, Hennig J, Unger C, and Marmé D.PTK787/ZK 222584, a specific vascular endothelial growth factor-receptor tyrosine kinase inhibitor, affects the anatomy of the tumor vascular bed and the functional vascular properties as detected by dynamic enhanced magnetic resonance imaging.Cancer Res62: 4015–4022, 2002.

10.1172/JCI17423

10.1083/jcb.140.4.947

10.1679/aohc.61.17

10.1007/s004180050328

10.1038/380439a0

10.1038/nm0398-336

10.1111/j.1600-0463.2004.apm11207-0809.x

Fong TA, Shawver LK, Sun L, Tang C, App H, Powell TJ, Kim YH, Schreck R, Wang X, Risau W, Ullrich A, Hirth KP, and McMahon G.SU5416 is a potent and selective inhibitor of the vascular endothelial growth factor receptor (Flk-1/KDR) that inhibits tyrosine kinase catalysis, tumor vascularization, and growth of multiple tumor types.Cancer Res59: 99–106, 1999.

Gerber HP, Hillan KJ, Ryan AM, Kowalski J, Keller GA, Rangell L, Wright BD, Radtke F, Aguet M, and Ferrara N.VEGF is required for growth and survival in neonatal mice.Development126: 1149–1159, 1999.

10.1073/pnas.95.15.8795

10.1038/315115a0

10.1073/pnas.172398299

Hu-Lowe D, Heller D, Brekken J, Feely R, Amundson K, Haines M, Troche G, Kim Y, Gonzalez D, Herrman M, Batago M, Vekich S, Kania R, McTigue M, Gregory S, Bender S, and Shalinsky D.Pharmacological activities of AG-013736, a small molecule inhibitor of VEGF/PDGF receptor tyrosine kinases.Proc Am Assoc Cancer Res43: A5357, 2002.

10.1073/pnas.1432908100

10.1056/NEJMoa032691

10.1016/S0002-9440(10)63273-7

10.1016/S1535-6108(02)00031-4

10.1152/ajpheart.00011.2003

10.1038/nm0901-987

10.1172/JCI10259

10.1152/ajpendo.2000.278.1.E1

10.1038/362841a0

10.1620/tjem.195.43

10.1073/pnas.081615298

Laird AD, Vajkoczy P, Shawver LK, Thurnher A, Liang C, Mohammadi M, Schlessinger J, Ullrich A, Hubbard SR, Blake RA, Fong TAT, Strawn LM, Sun L, Tang C, Hawtin R, Tang F, Shenoy N, Hirth KP, McMahon G, and Cherrington JM.SU6668 is a potent antiangiogenic and antitumor agent that induces regression of established tumors.Cancer Res60: 4152–4160, 2000.

10.1016/S0960-9822(03)00378-6

10.1210/en.2002-0146

10.1056/NEJMoa031884

10.2337/diabetes.51.8.2450

10.1172/JCI17189

10.1016/S0140-6736(03)13603-3

10.1038/sj.ijo.0802265

10.1152/ajpheart.2001.281.3.H1104

Palade GE, Simionescu M, and Simionescu N.Structural aspects of the permeability of the microvascular endothelium.Acta Physiol Scand Suppl463: 11–32, 1979.

10.1002/(SICI)1097-0142(19991201)86:11<2406::AID-CNCR31>3.0.CO;2-E

10.1096/fj.99-1049com

10.1111/j.1750-3639.1994.tb00835.x

10.1038/nbt1004-1198

Renkin EM.Relation of capillary morphology to transport of fluid and large molecules: a review.Acta Physiol Scand Suppl463: 81–91, 1979.

Roberts WGand Palade GE.Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor.J Cell Sci108: 2369–2379, 1995.

10.1158/1078-0432.CCR-040023

10.1016/0006-8993(86)91011-5

10.1074/jbc.273.45.29979

Simionescu Mand Simionescu N.Ultrastructure of the microvascular wall: functional correlations. In:Microcirculation: Part 1, edited by Renkin EM and Michel CC. Bethesda, MD: Am. Physiol. Soc. 1984, p. 41–101.

10.1016/S0022-5320(84)90178-3

10.1097/01.ASN.0000033277.32822.23

10.1073/pnas.96.23.13203

10.1091/mbc.E03-08-0593

10.1002/path.1805

10.1074/jbc.C300012200

10.1016/S0002-9440(10)65392-8

Vuorela P, Helske S, Hornig C, Alitalo K, Weich H, and Halmesmaki E.Amniotic fluid-soluble vascular endothelial growth factor receptor-1 in preeclampsia.Obstet Gynecol95: 353–357, 2000.

10.1177/002215540205000603

10.1177/002215540405200105

10.1023/A:1006094117427

10.1210/endo.143.7.8886

10.1056/NEJMoa021491

10.1016/S0024-3205(99)00314-8

10.1073/pnas.93.25.14765

10.1023/A:1021540120521

10.1016/S0002-9440(10)62567-9